Specific Environmental Temperature and Relative Humidity Conditions and Grafting Affect the Persistence and Dissemination of Salmonella enterica subsp. enterica Serotype Typhimurium in Tomato Plant Tissues

Abstract

Tomatoes are one of the most widely produced vegetables around the world; however, fresh tomatoes have been connected to multiple wide-scale salmonellosis outbreaks over the past decades. Salmonella is commonly found in the environment and can persist in hostile conditions for several weeks before being internalized into plant tissues, where it is protected from conventional sanitation methods. In addition to biotic factors (host, inoculum size, and phytobiome), abiotic factors (environmental conditions) may affect the persistence of Salmonella in crop production. This study demonstrates that specific environmental conditions, the inoculation method, and the inoculum density affect the persistence and dissemination of JSG626 in tomato plant tissues. Our findings enhance the understanding of interactions between Salmonella enterica and fresh produce and may lead to the development of novel management practices on farms. ABSTRACT Little is known about the abiotic factors contributing to the preharvest persistence of Salmonella in tomato tissues. Therefore, we investigated the effects of specific environmental conditions and contamination methods on the persistence and dissemination of Salmonella enterica subsp. enterica serotype Typhimurium (JSG626) in tomato plants. When plants were sprayed on the leaves with a JSG626-contaminated solution, JSG626 persistence in the phyllosphere (bacteria located on the surface of the inoculated foliage and stem tissues) was lower at higher temperatures (30°C day/25°C night) than at lower temperatures (20°C day/15°C night). However, wounding cotyledons with contaminated tools improved JSG626 persistence and the internalization rate (2.27%) in planta compared to spray inoculation (0.004%). The systemic dissemination of JSG626 to other tissues increased when contaminated plants were grown under low relative humidity (<40%); however, JSG626 was only detected in the root systems at later sampling times (between 21 and 98\u2009days postinoculation [dpi]). Further, after tomato scions were grafted onto rootstocks using contaminated cutting tools, dissemination of JSG626 was preferentially basipetal and occasionally acropetal in the plants, with higher persistence rates and loads of JSG626 in root systems compared to foliar tissues. JSG626 was detected in the grafting point and root systems up to 242 dpi; however, none of the fruits harvested from contaminated plants between 90 and 137 dpi were positive for JSG626. This study demonstrates that environmental temperature and relative humidity could be good indicators for estimating the persistence of Salmonella enterica in tomato plants. Further, root systems may represent a risk for long-term persistence of Salmonella enterica in tomato plants. IMPORTANCE Tomatoes are one of the most widely produced vegetables around the world; however, fresh tomatoes have been connected to multiple wide-scale salmonellosis outbreaks over the past decades. Salmonella is commonly found in the environment and can persist in hostile conditions for several weeks before being internalized into plant tissues, where it is protected from conventional sanitation methods. In addition to biotic factors (host, inoculum size, and phytobiome), abiotic factors (environmental conditions) may affect the persistence of Salmonella in crop production. This study demonstrates that specific environmental conditions, the inoculation method, and the inoculum density affect the persistence and dissemination of JSG626 in tomato plant tissues. Our findings enhance the understanding of interactions between Salmonella enterica and fresh produce and may lead to the development of novel management practices on farms.